The Journal of Neuroscience, September 15, 2002, 22(18):8071-8083
Three Functionally Distinct Adhesions in Filopodia: Shaft
Adhesions Control Lamellar Extension
Michael B.
Steketee1 and
Kathryn W.
Tosney1, 2
1 Neuroscience Program and 2 Department of
Molecular, Cellular, and Developmental Biology, The University of
Michigan, Ann Arbor, Michigan 48109
In this study, adhesions on individual filopodial shafts were shown
to control veil (lamellar) advance and to be modulated by guidance
cues. Adhesions were detected in individual filopodia of sensory growth
cones using optical recordings, adhesion markers, and electron
microscopy. Veils readily advanced along filopodia lacking shaft
adhesions but rarely advanced along filopodia displaying shaft
adhesions. Experiments altering adhesion showed that this relationship
is not caused by veils removing adhesions as they advanced. Reducing
adhesion with antibodies decreased the proportion of filopodia with
shaft adhesions and coordinately increased veil advance. Moreover, the
inhibitory relationship was maintained: veils still failed to advance
on individual filopodia that retained shaft adhesions. These results
support the idea that shaft adhesions inhibit veil advance. Of
particular interest, guidance cues can act by altering shaft adhesions.
When a cellular cue was contacted by a filopodial tip, veil extension
and shaft adhesions altered in concert. Contact with a Schwann cell
induced veil advance and inhibited shaft adhesions. In contrast,
contact with a posterior sclerotome cell prohibited veil advance and
promoted shaft adhesions. These results show that veil advance is
controlled by shaft adhesions and that guidance signal cascades can
alter veil advance by altering these adhesions. Shaft adhesions thus
differ functionally from two other adhesions identified on individual
filopodia. Tip adhesions suffice to signal. Basal adhesions do not
influence veil advance but are critical to filopodial initiation and
dynamics. Individual growth cone filopodia thus develop three
functionally distinct adhesions that are vital for both motility and navigation.
Key words:
adhesion; filopodia; growth cone; guidance; lamella; Schwann; sclerotome
Copyright © 2002 Society for Neuroscience 0270-6474/02/22188071-13$05.00/0
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